Mechanical stretch and shear flow induced reorganization and recruitment of fibronectin in fibroblasts

Scientific Reports

Volumn 1, Issue , 2011, Pages

  Steward, Robert L ^a   Cheng, Chao Min ^b   Ye, Jonathan D ^c   Bellin, Robert M ^c   Leduc, Philip R ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c Department of Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL; ARTICLE; BIOMECHANICS; CELL STRAIN 3T3; CHEMISTRY; CONFOCAL MICROSCOPY; DRUG ANTAGONISM; FIBROBLAST; FLOW KINETICS; FLUORESCENCE MICROSCOPY; IMAGE PROCESSING; MECHANICAL STRESS; MOUSE; PHYSIOLOGY; SHEAR STRENGTH; ULTRASTRUCTURE;

ANIMALS; BIOMECHANICS; FIBROBLASTS; FIBRONECTINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NIH 3T3 CELLS; RHEOLOGY; RHO GTP-BINDING PROTEINS; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 84859762844     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00147     Document Type: Article

References (52)

1. Lam, S. et al. Glucose-induced fibronectin and collagen type III expression in renal fibroblasts can occur independent of TGF-beta1. Kidney Int 63, 878-888 (2003). (Pubitemid 36315565)
2. Midwood, K. S., Valenick, L. V., Hsia, H. C. & Schwarzbauer, J. E. Coregulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol Biol Cell 15, 5670-5677 (2004). (Pubitemid 39564757)
3. Yamada, K. Cell surface interactions with extracellular materials. Ann. Rev. Biochem. 52, 761-799 (1983). (Pubitemid 13030693)
4. Wierzbicka-Patynowski, I. & Schwarzbauer, J. E. The ins and outs of fibronectin matrix assembly. J Cell Sci 116, 3269-3276 (2003). (Pubitemid 37038975)
5. Woods, A., Longley, R. L., Tumova, S, Couchman, J. R. Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch. Biochem. and Biophys 374, 66-72 (2000). (Pubitemid 30084409)
6. Wierzbicka-Patynowski, I. & Schwarzbauer, J. E. Regulatory role for SRC and phosphatidylinositol 3-kinase in initiation of fibronectin matrix assembly. J Biol Chem 277, 19703-19708 (2002). (Pubitemid 34967486)
7. Hynes, R. Molecular biology of fibronectin. Annu Rev Cell Biol 1, 67-90 (1985).
8. Ohashi, T., Kiehart, D. P. & Erickson, H. P. Dual labeling of the fibronectinmatrix and actin cytoskeleton with green fluorescent protein variants. J Cell Sci 115, 1221-1229 (2002). (Pubitemid 34272486)
9. Birchmeier, C., Kreis, T. E., Eppenberger, H. M., Winterhalter, K. H. & Birchmeier, W. Corrugated attachment membrane in WI-38 fibroblasts: alternating fibronectin fibers and actin-containing focal contacts. Proc Natl Acad Sci USA 77, 4108-4112 (1980). (Pubitemid 10022558)
10. Bourdoulous, S., Orend, G., MacKenna, D. A., Pasqualini, R. & Ruoslahti, E. Fibronectin matrix regulates activation of RHO and CDC42 GTPases and cell cycle progression. J Cell Biol 143, 267-276 (1998). (Pubitemid 28480534)
11. Hall, A. Rho GTPases and the actin cytoskeleton. Science 279, 509-514 (1998). (Pubitemid 28067271)
12. Hall, A. & Nobes, C. D. Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc Lond B Biol Sci 355 (2000).
13. Zhang, Q., Peyruchaud, O., French, K. J., Magnusson, M. K. & Mosher, D. F. Sphingosine 1-phosphate stimulates fibronectin matrix assembly through a Rhodependent signal pathway. Blood 93, 2984-2990 (1999). (Pubitemid 29200790)
14. Zhang, Q., Magnusson, M. K. & Mosher, D. F. Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-dependent actin stress fiber formation and cell contraction. Mol Biol Cell 8, 1415-1425 (1997). (Pubitemid 27385566)
15. Reddy, K. & Ross, J. M. Shear stress prevents fibronectin binding proteinmediated Staphylococcus aureus adhesion to resting endothelial cells. Infect Immun 69 (2001).
16. Larsen, M., Wei, C. & Yamada, K. M. Cell and fibronectin dynamics during branching morphogenesis. J Cell Sci 119, 3376-3384 (2006). (Pubitemid 44405222)
17. Trinh, L. A. & Stainier, D. Y. Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev Cell 6, 371-382 (2004). (Pubitemid 38364569)
18. Sottile, J., Hocking, D. C. & Swiatek, P. J. Fibronectin matrix assembly enhances adhesion-dependent cell growth. J Cell Sci 111 ( Pt 19), 2933-2943 (1998). (Pubitemid 28495200)
19. Niklason, L. E. et al. Functional arteries grown in vitro. Science 284, 489-493 (1999). (Pubitemid 29289622)
20. Fornaro, M. et al. Fibronectin protects prostate cancer cells from tumor necrosis factor-alpha-induced apoptosis via the AKT/survivin pathway. J Biol Chem 278, 50402-50411 (2003). (Pubitemid 37548884)
21. Bellin, R. M. et al. Defining the role of syndecan-4 in mechanotransduction using surface-modification approaches. Proc Natl Acad Sci USA 106, 22102-22107 (2009).
22. Chien, S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 292, H1209-1224 (2007). (Pubitemid 46377111)
23. Owan, I. et al. Mechanotransduction in bone: osteoblasts are more responsive to fluid forces than mechanical strain. Am J Physiol 273, C810-815 (1997).
24. Lin, Y. W., Cheng, C. M., Leduc, P. R. & Chen, C. C. Understanding sensory nerve mechanotransduction through localized elastomeric matrix control. PLoS One 4, e4293 (2009).
25. Cheng, C. M., Steward, R. L., Jr. & LeDuc, P. R. Probing cell structure by controlling the mechanical environment with cell-substrate interactions. J Biomech 42, 187-192 (2009).
26. Chou, S. Y., Cheng, C. M. & LeDuc, P. R. Composite polymer systems with control of local substrate elasticity and their effect on cytoskeletal and morphological characteristics of adherent cells. Biomaterials 30, 3136-3142 (2009).
27. Wang, J. H., Thampatty, B. P., Lin, J. S. & Im, H. J. Mechanoregulation of gene expression in fibroblasts. Gene 391, 1-15 (2007). (Pubitemid 46371351)
28. Mourgeon, E., Xu, J., Tanswell, A. K., Liu, M. & Post, M. Mechanical straininduced posttranscriptional regulation of fibronectin production in fetal lung cells. Am J Physiol 277, L142-149 (1999). (Pubitemid 29356761)
29. Defilippi, P. et al. Actin cytoskeleton organization in response to integrinmediated adhesion. Microsc Res Tech 47, 67-78 (1999). (Pubitemid 29474836)
30. Mitra, S. K., Hanson, D. A. & Schlaepfer, D. D. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6, 56-68 (2005). (Pubitemid 40064899)
31. Lerman, O. Z., Galiano, R. D., Armour, M., Levine, J. P. & Gurtner, G. C. Cellular dysfunction in the diabetic fibroblast: impairment in migration, vascular endothelial growth factor production, and response to hypoxia. Am J Pathol 162, 303-312 (2003). (Pubitemid 36042012)
32. Eastwood, M., McGrouther, D. A. & Brown, R. A. Fibroblast responses to mechanical forces. Proc Inst Mech Eng H 212, 85-92 (1998). (Pubitemid 128769985)
33. Danciu, T. E., Gagari, E., Adam, R. M., Damoulis, P. D. & Freeman, M. R. Mechanical strain delivers anti-apoptotic and proliferative signals to gingival fibroblasts. J Dent Res 83, 596-601 (2004). (Pubitemid 41766066)
34. Grierson, J. P. & Meldolesi, J. Shear stress-induced [Ca21]i transients and oscillations in mouse fibroblasts are mediated by endogenously released ATP. J Biol Chem 270, 4451-4456 (1995).
35. Garanich, J. S., Mathura, R. A., Shi, Z. D. & Tarbell, J. M. Effects of fluid shear stress on adventitial fibroblast migration: implications for flow-mediated mechanisms of arterialization and intimal hyperplasia. Am J Physiol Heart Circ Physiol 292, H3128-3135 (2007). (Pubitemid 47084568)
36. Galante, L. L. & Schwarzbauer, J. E. Requirements for sulfate transport and the diastrophic dysplasia sulfate transporter in fibronectin matrix assembly. J Cell Biol 179, 999-1009 (2007). (Pubitemid 350223494)
37. Phan-Thanh, L., Robert, L., Derouette, J. C. & Labat-Robert, J. Increased biosynthesis and processing of fibronectin in fibroblasts from diabetic mice. Proc Natl Acad Sci USA 84, 1911-1915 (1987). (Pubitemid 17054119)
38. Roy, S., Sala, R., Cagliero, E. & Lorenzi, M. Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with amemory. Proc Natl Acad SciUSA 87, 404-408 (1990).
39. Darby, I. A., Bisucci, T., Hewitson, T. D. & MacLellan, D. G. Apoptosis is increased in a model of diabetes-impaired wound healing in genetically diabetic mice. Int J Biochem Cell Biol 29, 191-200 (1997). (Pubitemid 27096432)
40. Qian, Y., Feldman, E. & Pennathur, S., Kretzler, M., Brosius, F. C., 3rd. From fibrosis to sclerosis: mechanisms of glomerulosclerosis in diabetic nephropathy. Diabetes 57, 1439-1445 (2008).
41. Kubicek, J. D., Brelsford, S., Ahluwalia, P. & Leduc, P. R. Integrated lithographic membranes and surface adhesion chemistry for three-dimensional cellular stimulation. Langmuir 20, 11552-11556 (2004). (Pubitemid 40049629)
42. Steward, R. L., Jr., Cheng, C. M., Wang, D. L. & Leduc, P. R. Probing Cell Structure Responses Through a Shear and Stretching Mechanical Stimulation Technique. Cell BIochem Biophys 56, 115-124 (2009).
43. Richard, M. N., Deniset, J. F., Kneesh, A. L., Blackwood, D. & Pierce, G. N. Mechanical stretching stimulates smooth muscle cell growth, nuclear protein import, and nuclear pore expression through mitogen-activated protein kinase activation. J Biol Chem 282, 23081-23088 (2007). (Pubitemid 47311950)
44. Tsilibary, E. C. Microvascular basement membranes in diabetes mellitus. J Pathol 200, 537-546 (2003). (Pubitemid 36818254)
45. Brem, H. & Tomic-Canic, M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest 117, 1219-1222 (2007). (Pubitemid 46718408)
46. Bitar, M. S. Glucocorticoid dynamics and impaired wound healing in diabetes mellitus. Am J Pathol 152, 547-554 (1998). (Pubitemid 28106401)
47. Kanters, S. D. et al. Plasma levels of cellular fibronectin in diabetes. Diabetes Care 24, 323-327 (2001). (Pubitemid 32119132)
48. Loot, M. A. et al. Fibroblasts derived from chronic diabetic ulcers differ in their response to stimulation with EGF, IGF-I, bFGF and PDGF-AB compared to controls. Eur J Cell Biol 81, 153-160 (2002).
49. Albuquerque, M. L., Waters, C. M., Savla, U., Schnaper, H. W. & Flozak, A. S. Shear stress enhances human endothelial cell wound closure in vitro. AmJ Physiol Heart Circ Physiol 279, H293-302 (2000). (Pubitemid 30616673)
50. Brown, T. D. Techniques for mechanical stimulation of cells in vitro: a review. J Biomech 33, 3-14 (2000).
51. Yi, Q. & Coppolino, M. G. Automated classification and quantification of F-actin-containing ruffles in confocal micrographs. Biotechniques 40, 745-746 (2006).
52. Swedlow, J. R. Quantitative fluorescence microscopy and image deconvolution. Methods Cell Biol 72, 349-367 (2003).